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Attentional asymmetry in schizophrenia: controlled and automatic processes
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Attentional Asymmetry in Schizophrenia: Controlled and Automatic Processes Cameron S. Carter, Lynn C. Robertson, Marc R. Chaderjian, Linda J. Celaya, and Thomas E. Nordahl
Two versions of Posner's covert orienting task were administered to 14 drug-free schizophrenic patients and 12 normal controls. In the schizophrenic subjects, automatic orienting to exogenous cues in the right visual field was impaired. However, this lateralizing general deficit was not present when the schizophrenics were able to direct attention effor~fully in the second version of the task using endogenous cues. These findings support the hypothesis that there is a deficit in left hemispheric mechanisms mediating visual spatial attention in schizophrenia, However, when schizophrenics are given the opportunity to use an attentional strategy they are able to partially overcome this lateralized processing deficit.
Introduction Recent findings in cognitive neuroscience have allowed the development of specific hypotheses regarding the neurobiological substrates of abnormal cognitive functioning in psychiatric disorders. For example, based upon converging evidence from neuroanatomic, functional imaging, and cognitive studies it has been proposed (Early et al 1989) that visual field asymmetries in spatial attention in schizophrenia are mediated by the effects of reduced dopamine activity in the left ventral striatum upon an anterior attention system. In their original report of this asymmetry of spatial selective attention in schizophrenia, Posner et al (1988) suggested that the study of cognitive operations in spatial attention offer particular promise in developing functional anatomic models of psychopathology. Such tasks have dissectable cognitive components and are thought to involve discrete neuronal systems. The spatial attention task utilized by Posner et al (1988) to study covert orienting has been widely used, and considerable progress has been made in elucidating the neural systems contributing to performance in this task (Posner and Peterson 1990). For instance, two separate forms of visual spatial orienting have been demonstrated (Posner and Cohen 1984; Muller and Rabbitt 1989; Rafal et al 1989). In one form, cues occurring at the location of targets automatically summon attention to the target location,
From the Departmentsof Psychiatry (CSC, I.ER, MRC, IJC, TEN) and Neurology(I.~2R), University of California at Davis School of Medicine;the Veterans AdministrationMedical Center, Martinez, California (I~R), and the Donner Laboratory, Lawrence Berkeley Laboratory, University of California, Berkeley, California (TEN). Address reprint requests to Cameron S. Carter, M.D., Department of Psychiatry, University of California at Davis, Medical Center, 4430 V Street, Sacramento, CA 95817. Received October 16. 1991; revised Sanuery21, 1992. © 1992 Sceiety of Biological Psychiatry
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regardless of whether the cue has any inherent validity. This automatic facilitation of target detection occurs in the first 300 msec following appearance of the cue and is followed by an inhibition (referred to as inhibition of return). Inhibition of return is indicated by longer detection times for targets in the cued location than for targets occurring in locations opposite the cue, and theoretically reflects a bias in visual scanning toward the processing of novel stimuli (Posner and Cohen 1984). This form of cuing is known as exogenous cuing because brightening a peripheral box summons attention to the cued location automatically, independent of any effort or strategy on the part of the subject. In the second form of visual spatial attention, a cue that has strong predictive value for the locatton of the target is presented at the center of the visual field; this cue is typically an arrow pointing toward the probable location of the target. This second form of cuing is referred to as endogenous (because the symbolic meaning of the cue conveys information that the subject then uses to direct attention to the probable spatial location of the target), and is considered to reflect a controlled or effortful cognitive operation. There is no associated inhibition of return with endogenous cues (Rafal et al 1989). It has been argued that these two forms of cuing represent discrete and independent spatial selective attention mechanisms (Rafal et al 1989; Muller and Rabbitt 1989), and there is evidence that they involve separate neuronal systems (Rafal et al 1989). It has been suggested that controlled selective spatial attention is mediated by networks that include the posterior parietal cortex and frontal lobes (Posner et al 1984; Robertson et al 1988; Posner et al 1988) whereas automatic selective spatial attention is mediated by subcortical structures. The inhibition of return component of automatic covert visual orienting appears to be mediated by brainstem mechanisms closely linked to those controlling eye movements (Posner and Cohen 1984, Rafal et al 1989). According to Rafal et al (1989), these two forms of attentional orienting, acting in concert, allow us to search ourenvironmentstrategically, without being distracted l- repeated extraneous stimulation. In subjects with schizophrenia, Posner et al (1988) reported findings that suggested a left hemisphere attentional deficit. These authors (Posner et al 1988; Posner and Early 1990) found a performance asymmetry on the covert orienting task, with longer reaction times for targets appearing in the right visual field after attention had been cued to the left visual field in comparison with the opposite condition, where targets are presented to the left visual field after a cue appeared in the right visual field. This pattern of performance is similar to that seen in patients with lesions in the left parietal lobe (Posner et ai 1984). They hypothesized that these findings could be accounted for by pathology in a functional network consisting of left posterior parietal cortex, language processing centers in the frontal lobe, and dopaminergic projections from the ventral striatum (Posner et al 1988; Early et al 1989). Despite evidence that there appear to be two distinct forms of covert visual orienting, the majority of studies of visual spatial attention have not clearly distinguished between the two systems (Henderson 1991); this is true also for the above study. Posner et al employed peripheral (exogenous) cues in combination with a probability manipulation. Exogenous cues were presented with an 80% probability that the target would ai~pear in the cued location. As such, their findings are based upon a task that does not discriminate between the automatic and controlled forms of spatial attentional orienting. In the study reported below, we have dissected the task to examine both the automatic and controlled components, and used both tasks with a group of medication-free patients with schizo-
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Table 1. Comparison of Demographic Characteristics: Schizophrenics and Controls Schizophrenics (n ffi 14) Mean age (years) Parents education (mean years) Gender (male/female)
31.6 (5.0) 13.2 (2.0) 1 I/3
Controls (n ffi 12) 30.9 (5.8) 14.2 (2.3)
NS ° NS b
9/3
NS ~
Standard deviations are given in parenthesis. aUnpaired t-test, df = 24, t = 0.74, p =" 0.74. bUnpaired t-test, (If = 24, t = - l.l,~,p = 0.25. ~ , df = I, X2 ffi 0.046, p = 0.80.
phrenia and with a group of normal controls. In doing so we sought a more precise understanding of the nature of the asymmetry of selective visual attention in schizophrenia. If successful, the findings may provide further constraints for the construction of functional-anatomic models of the attentional pathology in this disorder.
Methods
Subjects Participants consisted of 14 outpatients in an investigational drug protocol in the Department of Psychiatry at the University of California at Davis Medical Center. All met DSM-III-R criteria for schizophrenia on structured interview (SCID, Spitzer and Williams 1987) and had been off antipsychotic medications for at least 2 weeks prior to testing. Two patients had been previously treated with haloperidol decanoate and had received their last shot 9 and l0 weeks before testing. One patient had been receiving fluphenazine decanoate and had received his last shot I l weeks prior to testing. Some patients had continued to use anticholinergic medications for up to 4 days prior to testing and seven patients had used short-acting benzodiazepines, chloral hydrate, or benadryl intermittently during the washout period. Subjects using these latter agents were drug free for 24 hr prior to testing. Patients were screened for illicit drug use during the period of the study by history and by random urine screening. Patients using drugs illicitly during the week prior to testing were excluded from the sample. All but one patient were chronic and the group had been ill for a mean period of 9.5 (SD 6.5) years. They scored in the mild-tomoderate range on core-positive and negative symptom items on the Brief Psychiatric Rating Scale (Kane et al 1988). Twelve normal controls were recruited by advertisement and had no lifetime histories of mental disorder, no first-degree family history of psychotic: disorder, and no recent history of illicit drug use. Control subjects were matched with patients for age, gender, and years of parent's education (to match for familial socioeconomic status). As can be seen in Table l, the two groups were well matched on these variables. There was one left-handed subject in each of the two groups. All subjects had vision corrected to at least 20:30, evaluated by Snellen chart on the day of testing. Both patients and controls were paid for their participation. All subjects gave written informed consent prior to testing.
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Tasks Stimuli were presented on a Princeton color monitor controlled by an Everex 386 SI personal computer. Response timing was to 1 msec resolution and was controlled by the 8253 chip. Status of the response keys was monitored through the game port. Stimulus timing was tied to the vertical sync pulse. For both tasks, subject's heads were immobilized in a chin rest 540 mm from the monitor screen. Normal room illumination was used, a polaroid CP-50 glare protector was in place on the monitor, and the screen luminance was adjusted for comfort before the first subject was tested and remained fixed throughout the study. Subjects fixated on a central cross (X) and eye movements were monitored by direct observation. The two tasks were performed on t~:=¢same day in fi:.ed order, with the exogenous task followed by the endogenous task. The order was not counterbalanced because we did not want to introduce a bias in the exogenous task from a prior probability meaning for a cue in the endogenous task. A brief break was given between tasks.
Experiment 1: Exogenous Cuing. Two dimly lit boxes appeared throughout the block of trials 50 to the left and right of a central fixation cross (X). Cuing consisted of brightening of one of the boxes for 300 msec. The target (an asterisk) appeared in one of these boxes and subtended a visual angle of 0.5°; the visual angle of each box was I °. The cue and target were orthoganally varied and could occur on the left or the right with equal probability. In one-third of the trials, both boxes would brighten simultaneously; these trials served as the "neutral" cuing condition. As in Posner et al's (1988) study, presentation of targets followed cues at one of two intervals, 100 msec or 800 msec, with eq'mi probability. The target remained present until the subject responded. The subject's task was to respond as rapidly as possible to the appearance of a target by pressing a response button with the index finger of the dominant hand. Responses occurring before target presentation generated a "too soon" message, and these trials were repeated in a later trial. Four blocks of 48 trials were presented with brief breaks between each block, Three filler trials at the beginning of each block were also included but omitted from the analysis. One block of 48 practice trials preceded the experimental trials. Experiment 2: Endogenous Cuing. The fixation and target parameters were the same as for the exogenously cued task. Throughout the experiment the peripheral boxes remained dimly illuminated. In this version of the covert orienting task, the cue consisted of a brightening of one or the other half of the fixation cue for 300 msec. When the left side (>) of the fixation cross brightened pointing towards the right, this indicated an 80% probability that the target would appear in the right-sided box. When the right side of the fixation cross brightened (<) pointing towards the left, this indicated an 80% probability that the target would appear in the left-sided box. Each brightened arrow cue subtended a visual angle of 0.5 °. On one-third of the trials, both sides of the fixation cross brightened; this served as the "neutral" cuing condition. As in Experiment 1, subjects responded by pressing a response button to indicate target detection; the ~::~rget~em~tned present until the subject responded. Premature responses elicited a "too soon" message and these trials were repeated. Subjects completed 4 blocks of 120 trials ~vithbrief breaks between blocks. Subjects completed a block of 60 practice trials prior to the experimental trials, and 3 filler trials were presented at the beginning of each block ~nd omitted from the analysis.
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Analysis For each experiment, median reaction times (RT) for each subject were calculated for each cell of the design, with group as the between-subjects factor and cue condition (neutral, valid, and invalid), target field (left, right), and cue target interval (100 msec, 800 msec) as within-subject factors. These were analyzed by an analysis of variance (ANOVA) for mixed design. There were several planned comparisons, includiag group by target field and costs and benefits within ant! across each field for each group. We also expected an inhibition of return effect for exogenous cuing prompting, a planned comparison of the 100 and 800 msec cue target intervals separately for Experiment 1. Benefits (the reaction time advantage obtained from valid cuing) were calculated by comparing reaction times of validly and neutrally cued targets for the left and right visual fields, respectively. Costs (the reaction time disadvantage of being cued to the opposite field to where the target appears) were calculated by comparing the reaction ~.imes of neutrally cued trials from those of invalidly cued trials.
Results Subjects were able to correct any tendency to move their eyes away from the fixation point during the practice trials. One patient with schizophrenia made saccades on less than 3% of trials during the exogenous cuing task. No eye movements were observed in any other subjects during this task and no subjects made eye movements during the exogenous cuing task. The cuing effects reported below, therefore, reflect the covert orienting of visual spatial attention.
Exogenous Cues Despite the fact that the probability of the target appearing at the cued location was 0.5, exogenous cues effectively changed performance, producing an overall main effect of validity, F ( 2 , 4 8 ) - 12.91, p < 0.001. As expected, RT at 800 msec was faster than at 100, F (1,24) -- 21.03, p < 0.001, and given that exogenous cues produce inhibition of return (Posner and Cohen 1984), there was a validity by interval interaction, F (2,48) -- 34.01, p < 0.001. This effect did not differ for the two groups. However, there was a significant interval by target field interaction, F (1,24) = 11.95, p < 0.01, and a significant group by interval by target field interaction, F (1,24) - 6.24, p < 0.02. The mean reaction times for patient and control groups, for each cue type, and for each of the two intervals are shown in Figure 1. There was no difference between fields for either group at the 800 msec interval and there were no field differences at 100 msec for controls, F < 1. However, right visual field responses were overall longer than left visual field responses for schizophrenic patients at the 100 msec interval, F (1,13) = 5.26, p < 0.04. Finally, there was a significant validity by field effect in the overall validity analysis F (2,48) - 5.95 p < 001. Because the costs and benefits at the 800-msec interval reflected inhibition of return, which did not differ between groups, costs and benefits were analyzed for the 100-msec interval only. Analysis of costs between groups for the 100-msec cue-target interval revealed significant costs, F (1,24) - 4.77, p < 0.04. There was a trend towards a main effect of group, F (1,24) -- 3.70, p = 0.07 suggesting that response times overall were longer in schizophrenics. There was also a significant validity by field effect, F (1,24) = 8.17, p < 0.01. Thus, there were greater costs for left visual field targets than right
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450 1
,....o
4oo
Schizophrenics
E
Controls
i °0 I
[
450 400
,....'=t.
350 300
Left visual field ...... Right visual field I I I 250 / , i i 250 Neutral Valid Invalid Neutral Valid Invalid 100 msee 8OA 800 meee SOA Cue Condition I
Figure !. Exogenous cues: mean reaction times of schi~,i: enic subjects and controls for each cue condition at the 100 and 800 msec cue target interval .
visual field targets at this cue target interval. However, this did not differ between groups, F (1,24) = 1.76p = 0.20. For benefits, there was a main effect of validity, F (1,24) - 12.17, p < 0.01, and a main effect of field, F (! ,24) = 10.57, p < 0.01, showing that left visual field targets were responded to faster than right visual field targets overall. Again, there was a tendency toward longer response times for schizophrenics overall, evidenced by a trend towards a main effect of group, F (1,24) = 3.24, p -- 0.08. There were no higher order interactions. Because the results of the cost-benefit analysis as undertaken here depends upon the nature of the neutral condition (Jonides and Mack 1984), we also performed an analysis comparing valid to invalid cue conditions. Using this approach we found a main effect for validity, F (1,24) = 12.99, p < 0.01, and a trend towards longer reaction times for schizophrenics, F (1,24) = 3.77, p = 0.06. The field by group interaction was significant, F (1,24) = 4.82, p < 0.04. Schizophrenics produced longer reaction times for targets in the right visual field but normals did not. There was no validity by group interaction, F < 1, and no validity by field by group interaction. Using both approaches to the cost-benefit analysis, the overall pattern of costs and benefits in the automatic orienting of attention is similar in both schizophrenic patients and normal controls. However, schizophrenics' performance was different from normals over visual fields. They demonstrated a left visual field advantage that was not present in normals; it was present at the 100-msec cue target interval but not at the 800-msec cue target interval suggesting that there is tic general disruption of responding to right visual field stimuli in these patients, but that the process of automatically orienting to right visual field stimuli is slower in this group.
Endogenous Cues Endogenous cues with an 80:20 probability produced the normal main effect of validity, F (2,48) = 9.48, p < 0.001, and cue target interval, F (1,24) = 55.68, p < 0.001. The validity effect differed over field, F (2,48) = 3.39, p < 0.05, and this effect differed
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450
i
Schizophrenics / 400
J~ . , , ,_.....0 ,~
-
4) ~- 350
g
Controls
300 ...... 250
Figure 2. Endogenous cues: mean reaction times of schizophrenic subjects and controls for each cue condition. Loft visualfield Flightvisualfield
I
I
i
Neutral
Vatld
Invalid
Cue CondlUon
across groups, F (2,48) ffi 3.63, p < 0.03. As with the trend observed with exogenous cues, schizophrenics were overall slower than normals, F (1,24) ffi 4.68, p < 0.04, but there was no hint of an interval by field interaction nor an interval by field by group interaction, F < 1. Further group comparisons were therefore made collapsed across cuetarget interval. Mean reaction times for each cue condition for the two groups are presented in Figure 2. Analysis of costs (neutral versus invalid cue) revealed a main effect of validity, F (1,24) - 4.91, p ffi < 0.04, and a main effect of group, F (1,24) ffi 4.62, p < 0.04, with schizophrenic subjects once again showing longer reaction times overall. There was also a trend towards a significant group by field by validity interaction, F (1,24) = 3.52, p ffi 0.07. Because a left field advantage in schizophrenia has been hypothesized, we evaluated this trend with planned comparisons. For schizophrenic subjects there were significant costs for left visual field targets F (1,13) ffi 5.15, p ffi 0.04, whereas for right visual field targets no costs were evident, F < 1. In normals, significant costs were seen for targets in the right visual field, F (1,11) ffi 8.10, p < 0.02 but there was only a trend toward costs for left visual field targets, F (1,11) ffi 3.37, p ffi 0.09. In the analysis of benefits (neutral versus valid trials), there was a main effect of validity, F (1,24) ffi 36.24, p < 0.001, and again a main effect of group, F (1,24) 4.66, p < 0.04, with schizophrenics having longer reaction times overall than controls. No hint of a group by field by validity interaction was present, F < 1, NS. These findings suggest a performance asymmetry for effortful covert orienting in this group of schizophrenic subjects characterized by greater costs to invalidly cued left vi~,~ual field targets than to invalidly cued targets appearing in the right visual field. However, the right visual field disadvantage found with exogenous cues disappeared for neutral and valid conditions and was reversed for the invalid condition.
Discussion The results for the exogenous task provide further evidence for the presence of a left hemispheric deficit in information processing in schizophrenia. An analysis of the source of the significant group by field by interval interaction in the exogenously cued task
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indicated that automatic orienting to targets presented in the fight visual field at the 100msec interval was slower in schizophrenics than in normals. This finding is consistent with a deficit in visual spatial orienting mediated by the left hemisphere. The schizophrenic subjects in this study, who were all off medications, did not automatically attend to cues in the peripheral right visual field as readily as to cues in the left visual field. However, the pattern of performance with endogenous cuing suggests that the schizophrenic patients were able to use symbolic cues to control attention and largely overcome this particular lateraiized deficit. A possible confound in the comparison of the results of the two tasks in the current study is that their order of administration to subjects was not counterbalanced. This raises the possibility of fatigue leading to differential performance on the two tasks. As discussed in the Methods section, we did not counterbalance tasks to avoid biasing performance in the exogenously cued task with a prior probability manipulation. As the more general right visual field deficit reported here is seen with the exogenously cued task, which was given first, this particular finding is not subject to this potential confound. The findings with endogenous cues are consistent with those of Posner et al (1988) for validly cued conditions where these authors compared their findings to those obtained from studies of patients with lesions of the parietal lobe. Such patients can overcome contralesional delays when they are cued to the target location. Ever~ patients with full blown neglect can do so in validly cued trials (Morrow and Ratcliffc 1987). The ability to effortfully use attention is relatively intact in these neurologically damaged patients (Posner et al 1984). However, the pattern of asymmetry of costs for invalidly cued targets seen with endogenous cues is different from that reported in left parietal patients and different from that ~eported by Posner et al (1988) in their study of patients with schizophrenia. In left parietal patients, and in the schizophrenic subjects studied by Posner et al, costs were relatively larger for invalidly cued right visual field targets (left field cues) than invalidly cued left visual field targets (right field cues). In the present study the asymmetry in costs in the schizophrenic patients ran in the opposite direction, with greater costs for invalid left visual field targets than for invalid right visual field targets. There are a number of possible explanations for our finding a different pattern of asymmetry in costs to those reported in the Posner et al (1988) study. A recent report by Strauss et al (1991) of an absence of asymmetry of performance in a group of stable, treated and remitted schizophrenics suggests that cost asymmetry in the covert orienting task in schizophrenia may be a state-dependent phenomenon. All three untreated patients in the Posner et al (1988) study were subchronic or schizophreniform at the time of testing. The rest of the patients were subchronic or chronic and treated with a variety of medications. All patients were acutely psychotic. Tomer and Flor-Henry (1989) have demonstrated a reversal of asymmetrical hemi-neglect in acutely psychotic schizophrenic patients following a brief course of treatment with neuroleptic agents, with an initial right field deficit evolving into a left field deficit with drug treatment. Patients with Parkinsons disease (Wright et al 1990) and young normal subjects challenged with the neuroleptic droperidol (Clark et al 1988) show decreased costs associated with invalid cues when compared with normals and placebo challenges, respectively. Variability in dopamine activity during the course of the illness, with clinical state, or associated with the effects of treatment may account for the reversed asymmetry in costs which contrasts our findings with endogenous cues and the findings of Posner et al )88). Further studies comparing patients with schizopl ala at different phases in their
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illness, prospective studies of patients on and off medications, and studies of normals challenged with both dopamine agonist and antagonist drags, are needed to c,arify the role of each of the above factors in determining the pattern of costs and benefits in endogenously cued covert orienting of attention. Such studies are currently being initiated in our laboratory. Finally, a number of differences between our endogenous cuing paradigm and that used by Posner et al do not make the current study entirely comparable with previous studies. In the current study we used a neutral cue consisting of brightening of both central directional cues, whereas Posner et al (1988) used a no cue condition. It is possible that the occasional absence of a cue (as compared with simultaneous presence of both directional cues) may have produced a higher level of attentiveness in the Posner et al (1988) study. Posner's no cue condition was also less probable (20% of trials) than our neutral cue condition (one-third of trials), and this also could result in greater attentiveness in the former task. Higher levels of attentiveness may result in increased benefits and decreased costs for cues (Jonides and Mack 1984). Secondly, in contrast to the brightening of the peripheral boxes used by Posner et al, directional cues in the current study consisted of brightening of central directional cues. Thus, previous findings may reflect the effects of automatic visual orienting, inhibition of return, and controlled covert visual orienting, whereas the current study provides a more direct measure of automatic and controlled contributions to covertly directed visual spatial attention. These findings suggest that automatic orienting to endogenously cued targets is disrupted for right visual field targets in schizophrenia, consistent with left hemispheric attentional pathology in this illness. They also suggest that when schizophrenics are provided with cues that allow them to use attention strategically they are able to largely overcome this general right visual field attentional deficit. This study was supportedin part by VA MedicalResearchCouncilawardAA06637to LynnC. Robertsonand by NIMHGrant M.H. 46990 to Thomas E. Nordahl.
References Clark CR, Oeffen GM, Oeffen LB (1988): Catecholamines and the covert orientation of attention in humans. Neuropsychologia 27:131-139. Early TS, Posner MI, Reiman EM, Raichle ME (1989): Hyperactivity of the left striato-pallidal projection. Part I: Lower level theory. Psychol Dev 2:85-108. Henderson JM (1991): Stimulus discrimination following covert attentional orienting to an exogenous cue. J Exp Psychol 17(I):91-106. Jonides J, Mack R (1984): On the cost and benefit of cost and benefit. Psychol Bull 96(10:29-44. Kane J, Honigfield G, Singer J, Meltzer H (1988): Clozapine for the treatment-free schizophrenic. Arch Gen Psychiatry 45:789-796. Morrow LA, Ratcliffe G (1987): Attentional mechanisms in clinical neglect. J Clin Exp Neuropsychol 9:74-75. Muller HJ, Rabbitt P (1989): Reflexive and voluntary orienting of visual attention: Time course of activation and resistance to interruption. J Exp Psychol 15(2):315-330. Posner MI, Cohen Y (1984): Components of visual orienting. In Bouma H, Bouwhuis DG (eds), Attention and Performance. Hillsdale, NJ: Erlbaum, pp 531-556. Posner MI, Early TS (19°0): What's left of attention in schizophrenia. Arch Gen Psychiatry 47(4):394.
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Posner MI, Peterson SE (1990): The attention system of the human brain. Annu Rev Neurosci 13:25-42. Posner MI, Walker JA, Frieclrich FJ, Rafal RD (1984): Effects of parietal lobe injury on the covert orienting of visual attention. J Neurosci 4:1863-1874. Posner MI, Early TS, Reiman E, Pardo PJ, Dhawan M (1988): Asymmetries of attentional control in schizophrenia. Arch Gen Psychiatry 45:814-821. Rafai RD, Calahresi PA, Brennan CW, Sciolto TK (1989): Saccade preparation inhibits reorienting to recently attended locations. J Exp Psychol 15(4):673-685. Robertson LC, Lamb MR, Knight RT (1988): Effects of lesions of temporo-parietai junction on perceptual and attentional processing in humans. J Neurosci 10:3757-3769. Spitzer R, Williams JW (1987): Structured clinical interview for DSM-III, revised version. New York, NY: New York Psychiatric Institute. S~r~e~ ,~,~E,Novakovic T, Tien AY, Bylsma F, Pearlson GD (1991): Disengagement of attention in schizophrenia. Psychiatry Res 37:139-146. Tomer R, Flor-Henry P (1989): Neuroleptics reverse attention asymmetries in schizophrenic patients. Biol Psychiatry 25:852-860. Wright MJ, Bums RJ, Geffen GM, Geffen LB (1990): Covert orientation of visual attention in Parkinsons disease: An impairment in the maintenance of attention. Neuropsychologia 28(2):151159.
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Attentional Asymmetry in Schizophrenia: Controlled and Automatic Processes Cameron S. Carter, Lynn C. Robertson, Marc R. Chaderjian, Linda J. Celaya, and Thomas E. Nordahl
Two versions of Posner's covert orienting task were administered to 14 drug-free schizophrenic patients and 12 normal controls. In the schizophrenic subjects, automatic orienting to exogenous cues in the right visual field was impaired. However, this lateralizing general deficit was not present when the schizophrenics were able to direct attention effor~fully in the second version of the task using endogenous cues. These findings support the hypothesis that there is a deficit in left hemispheric mechanisms mediating visual spatial attention in schizophrenia, However, when schizophrenics are given the opportunity to use an attentional strategy they are able to partially overcome this lateralized processing deficit.
Introduction Recent findings in cognitive neuroscience have allowed the development of specific hypotheses regarding the neurobiological substrates of abnormal cognitive functioning in psychiatric disorders. For example, based upon converging evidence from neuroanatomic, functional imaging, and cognitive studies it has been proposed (Early et al 1989) that visual field asymmetries in spatial attention in schizophrenia are mediated by the effects of reduced dopamine activity in the left ventral striatum upon an anterior attention system. In their original report of this asymmetry of spatial selective attention in schizophrenia, Posner et al (1988) suggested that the study of cognitive operations in spatial attention offer particular promise in developing functional anatomic models of psychopathology. Such tasks have dissectable cognitive components and are thought to involve discrete neuronal systems. The spatial attention task utilized by Posner et al (1988) to study covert orienting has been widely used, and considerable progress has been made in elucidating the neural systems contributing to performance in this task (Posner and Peterson 1990). For instance, two separate forms of visual spatial orienting have been demonstrated (Posner and Cohen 1984; Muller and Rabbitt 1989; Rafal et al 1989). In one form, cues occurring at the location of targets automatically summon attention to the target location,
From the Departmentsof Psychiatry (CSC, I.ER, MRC, IJC, TEN) and Neurology(I.~2R), University of California at Davis School of Medicine;the Veterans AdministrationMedical Center, Martinez, California (I~R), and the Donner Laboratory, Lawrence Berkeley Laboratory, University of California, Berkeley, California (TEN). Address reprint requests to Cameron S. Carter, M.D., Department of Psychiatry, University of California at Davis, Medical Center, 4430 V Street, Sacramento, CA 95817. Received October 16. 1991; revised Sanuery21, 1992. © 1992 Sceiety of Biological Psychiatry
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regardless of whether the cue has any inherent validity. This automatic facilitation of target detection occurs in the first 300 msec following appearance of the cue and is followed by an inhibition (referred to as inhibition of return). Inhibition of return is indicated by longer detection times for targets in the cued location than for targets occurring in locations opposite the cue, and theoretically reflects a bias in visual scanning toward the processing of novel stimuli (Posner and Cohen 1984). This form of cuing is known as exogenous cuing because brightening a peripheral box summons attention to the cued location automatically, independent of any effort or strategy on the part of the subject. In the second form of visual spatial attention, a cue that has strong predictive value for the locatton of the target is presented at the center of the visual field; this cue is typically an arrow pointing toward the probable location of the target. This second form of cuing is referred to as endogenous (because the symbolic meaning of the cue conveys information that the subject then uses to direct attention to the probable spatial location of the target), and is considered to reflect a controlled or effortful cognitive operation. There is no associated inhibition of return with endogenous cues (Rafal et al 1989). It has been argued that these two forms of cuing represent discrete and independent spatial selective attention mechanisms (Rafal et al 1989; Muller and Rabbitt 1989), and there is evidence that they involve separate neuronal systems (Rafal et al 1989). It has been suggested that controlled selective spatial attention is mediated by networks that include the posterior parietal cortex and frontal lobes (Posner et al 1984; Robertson et al 1988; Posner et al 1988) whereas automatic selective spatial attention is mediated by subcortical structures. The inhibition of return component of automatic covert visual orienting appears to be mediated by brainstem mechanisms closely linked to those controlling eye movements (Posner and Cohen 1984, Rafal et al 1989). According to Rafal et al (1989), these two forms of attentional orienting, acting in concert, allow us to search ourenvironmentstrategically, without being distracted l- repeated extraneous stimulation. In subjects with schizophrenia, Posner et al (1988) reported findings that suggested a left hemisphere attentional deficit. These authors (Posner et al 1988; Posner and Early 1990) found a performance asymmetry on the covert orienting task, with longer reaction times for targets appearing in the right visual field after attention had been cued to the left visual field in comparison with the opposite condition, where targets are presented to the left visual field after a cue appeared in the right visual field. This pattern of performance is similar to that seen in patients with lesions in the left parietal lobe (Posner et ai 1984). They hypothesized that these findings could be accounted for by pathology in a functional network consisting of left posterior parietal cortex, language processing centers in the frontal lobe, and dopaminergic projections from the ventral striatum (Posner et al 1988; Early et al 1989). Despite evidence that there appear to be two distinct forms of covert visual orienting, the majority of studies of visual spatial attention have not clearly distinguished between the two systems (Henderson 1991); this is true also for the above study. Posner et al employed peripheral (exogenous) cues in combination with a probability manipulation. Exogenous cues were presented with an 80% probability that the target would ai~pear in the cued location. As such, their findings are based upon a task that does not discriminate between the automatic and controlled forms of spatial attentional orienting. In the study reported below, we have dissected the task to examine both the automatic and controlled components, and used both tasks with a group of medication-free patients with schizo-
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Table 1. Comparison of Demographic Characteristics: Schizophrenics and Controls Schizophrenics (n ffi 14) Mean age (years) Parents education (mean years) Gender (male/female)
31.6 (5.0) 13.2 (2.0) 1 I/3
Controls (n ffi 12) 30.9 (5.8) 14.2 (2.3)
NS ° NS b
9/3
NS ~
Standard deviations are given in parenthesis. aUnpaired t-test, df = 24, t = 0.74, p =" 0.74. bUnpaired t-test, (If = 24, t = - l.l,~,p = 0.25. ~ , df = I, X2 ffi 0.046, p = 0.80.
phrenia and with a group of normal controls. In doing so we sought a more precise understanding of the nature of the asymmetry of selective visual attention in schizophrenia. If successful, the findings may provide further constraints for the construction of functional-anatomic models of the attentional pathology in this disorder.
Methods
Subjects Participants consisted of 14 outpatients in an investigational drug protocol in the Department of Psychiatry at the University of California at Davis Medical Center. All met DSM-III-R criteria for schizophrenia on structured interview (SCID, Spitzer and Williams 1987) and had been off antipsychotic medications for at least 2 weeks prior to testing. Two patients had been previously treated with haloperidol decanoate and had received their last shot 9 and l0 weeks before testing. One patient had been receiving fluphenazine decanoate and had received his last shot I l weeks prior to testing. Some patients had continued to use anticholinergic medications for up to 4 days prior to testing and seven patients had used short-acting benzodiazepines, chloral hydrate, or benadryl intermittently during the washout period. Subjects using these latter agents were drug free for 24 hr prior to testing. Patients were screened for illicit drug use during the period of the study by history and by random urine screening. Patients using drugs illicitly during the week prior to testing were excluded from the sample. All but one patient were chronic and the group had been ill for a mean period of 9.5 (SD 6.5) years. They scored in the mild-tomoderate range on core-positive and negative symptom items on the Brief Psychiatric Rating Scale (Kane et al 1988). Twelve normal controls were recruited by advertisement and had no lifetime histories of mental disorder, no first-degree family history of psychotic: disorder, and no recent history of illicit drug use. Control subjects were matched with patients for age, gender, and years of parent's education (to match for familial socioeconomic status). As can be seen in Table l, the two groups were well matched on these variables. There was one left-handed subject in each of the two groups. All subjects had vision corrected to at least 20:30, evaluated by Snellen chart on the day of testing. Both patients and controls were paid for their participation. All subjects gave written informed consent prior to testing.
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Tasks Stimuli were presented on a Princeton color monitor controlled by an Everex 386 SI personal computer. Response timing was to 1 msec resolution and was controlled by the 8253 chip. Status of the response keys was monitored through the game port. Stimulus timing was tied to the vertical sync pulse. For both tasks, subject's heads were immobilized in a chin rest 540 mm from the monitor screen. Normal room illumination was used, a polaroid CP-50 glare protector was in place on the monitor, and the screen luminance was adjusted for comfort before the first subject was tested and remained fixed throughout the study. Subjects fixated on a central cross (X) and eye movements were monitored by direct observation. The two tasks were performed on t~:=¢same day in fi:.ed order, with the exogenous task followed by the endogenous task. The order was not counterbalanced because we did not want to introduce a bias in the exogenous task from a prior probability meaning for a cue in the endogenous task. A brief break was given between tasks.
Experiment 1: Exogenous Cuing. Two dimly lit boxes appeared throughout the block of trials 50 to the left and right of a central fixation cross (X). Cuing consisted of brightening of one of the boxes for 300 msec. The target (an asterisk) appeared in one of these boxes and subtended a visual angle of 0.5°; the visual angle of each box was I °. The cue and target were orthoganally varied and could occur on the left or the right with equal probability. In one-third of the trials, both boxes would brighten simultaneously; these trials served as the "neutral" cuing condition. As in Posner et al's (1988) study, presentation of targets followed cues at one of two intervals, 100 msec or 800 msec, with eq'mi probability. The target remained present until the subject responded. The subject's task was to respond as rapidly as possible to the appearance of a target by pressing a response button with the index finger of the dominant hand. Responses occurring before target presentation generated a "too soon" message, and these trials were repeated in a later trial. Four blocks of 48 trials were presented with brief breaks between each block, Three filler trials at the beginning of each block were also included but omitted from the analysis. One block of 48 practice trials preceded the experimental trials. Experiment 2: Endogenous Cuing. The fixation and target parameters were the same as for the exogenously cued task. Throughout the experiment the peripheral boxes remained dimly illuminated. In this version of the covert orienting task, the cue consisted of a brightening of one or the other half of the fixation cue for 300 msec. When the left side (>) of the fixation cross brightened pointing towards the right, this indicated an 80% probability that the target would appear in the right-sided box. When the right side of the fixation cross brightened (<) pointing towards the left, this indicated an 80% probability that the target would appear in the left-sided box. Each brightened arrow cue subtended a visual angle of 0.5 °. On one-third of the trials, both sides of the fixation cross brightened; this served as the "neutral" cuing condition. As in Experiment 1, subjects responded by pressing a response button to indicate target detection; the ~::~rget~em~tned present until the subject responded. Premature responses elicited a "too soon" message and these trials were repeated. Subjects completed 4 blocks of 120 trials ~vithbrief breaks between blocks. Subjects completed a block of 60 practice trials prior to the experimental trials, and 3 filler trials were presented at the beginning of each block ~nd omitted from the analysis.
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Analysis For each experiment, median reaction times (RT) for each subject were calculated for each cell of the design, with group as the between-subjects factor and cue condition (neutral, valid, and invalid), target field (left, right), and cue target interval (100 msec, 800 msec) as within-subject factors. These were analyzed by an analysis of variance (ANOVA) for mixed design. There were several planned comparisons, includiag group by target field and costs and benefits within ant! across each field for each group. We also expected an inhibition of return effect for exogenous cuing prompting, a planned comparison of the 100 and 800 msec cue target intervals separately for Experiment 1. Benefits (the reaction time advantage obtained from valid cuing) were calculated by comparing reaction times of validly and neutrally cued targets for the left and right visual fields, respectively. Costs (the reaction time disadvantage of being cued to the opposite field to where the target appears) were calculated by comparing the reaction ~.imes of neutrally cued trials from those of invalidly cued trials.
Results Subjects were able to correct any tendency to move their eyes away from the fixation point during the practice trials. One patient with schizophrenia made saccades on less than 3% of trials during the exogenous cuing task. No eye movements were observed in any other subjects during this task and no subjects made eye movements during the exogenous cuing task. The cuing effects reported below, therefore, reflect the covert orienting of visual spatial attention.
Exogenous Cues Despite the fact that the probability of the target appearing at the cued location was 0.5, exogenous cues effectively changed performance, producing an overall main effect of validity, F ( 2 , 4 8 ) - 12.91, p < 0.001. As expected, RT at 800 msec was faster than at 100, F (1,24) -- 21.03, p < 0.001, and given that exogenous cues produce inhibition of return (Posner and Cohen 1984), there was a validity by interval interaction, F (2,48) -- 34.01, p < 0.001. This effect did not differ for the two groups. However, there was a significant interval by target field interaction, F (1,24) = 11.95, p < 0.01, and a significant group by interval by target field interaction, F (1,24) - 6.24, p < 0.02. The mean reaction times for patient and control groups, for each cue type, and for each of the two intervals are shown in Figure 1. There was no difference between fields for either group at the 800 msec interval and there were no field differences at 100 msec for controls, F < 1. However, right visual field responses were overall longer than left visual field responses for schizophrenic patients at the 100 msec interval, F (1,13) = 5.26, p < 0.04. Finally, there was a significant validity by field effect in the overall validity analysis F (2,48) - 5.95 p < 001. Because the costs and benefits at the 800-msec interval reflected inhibition of return, which did not differ between groups, costs and benefits were analyzed for the 100-msec interval only. Analysis of costs between groups for the 100-msec cue-target interval revealed significant costs, F (1,24) - 4.77, p < 0.04. There was a trend towards a main effect of group, F (1,24) -- 3.70, p = 0.07 suggesting that response times overall were longer in schizophrenics. There was also a significant validity by field effect, F (1,24) = 8.17, p < 0.01. Thus, there were greater costs for left visual field targets than right
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450 1
,....o
4oo
Schizophrenics
E
Controls
i °0 I
[
450 400
,....'=t.
350 300
Left visual field ...... Right visual field I I I 250 / , i i 250 Neutral Valid Invalid Neutral Valid Invalid 100 msee 8OA 800 meee SOA Cue Condition I
Figure !. Exogenous cues: mean reaction times of schi~,i: enic subjects and controls for each cue condition at the 100 and 800 msec cue target interval .
visual field targets at this cue target interval. However, this did not differ between groups, F (1,24) = 1.76p = 0.20. For benefits, there was a main effect of validity, F (1,24) - 12.17, p < 0.01, and a main effect of field, F (! ,24) = 10.57, p < 0.01, showing that left visual field targets were responded to faster than right visual field targets overall. Again, there was a tendency toward longer response times for schizophrenics overall, evidenced by a trend towards a main effect of group, F (1,24) = 3.24, p -- 0.08. There were no higher order interactions. Because the results of the cost-benefit analysis as undertaken here depends upon the nature of the neutral condition (Jonides and Mack 1984), we also performed an analysis comparing valid to invalid cue conditions. Using this approach we found a main effect for validity, F (1,24) = 12.99, p < 0.01, and a trend towards longer reaction times for schizophrenics, F (1,24) = 3.77, p = 0.06. The field by group interaction was significant, F (1,24) = 4.82, p < 0.04. Schizophrenics produced longer reaction times for targets in the right visual field but normals did not. There was no validity by group interaction, F < 1, and no validity by field by group interaction. Using both approaches to the cost-benefit analysis, the overall pattern of costs and benefits in the automatic orienting of attention is similar in both schizophrenic patients and normal controls. However, schizophrenics' performance was different from normals over visual fields. They demonstrated a left visual field advantage that was not present in normals; it was present at the 100-msec cue target interval but not at the 800-msec cue target interval suggesting that there is tic general disruption of responding to right visual field stimuli in these patients, but that the process of automatically orienting to right visual field stimuli is slower in this group.
Endogenous Cues Endogenous cues with an 80:20 probability produced the normal main effect of validity, F (2,48) = 9.48, p < 0.001, and cue target interval, F (1,24) = 55.68, p < 0.001. The validity effect differed over field, F (2,48) = 3.39, p < 0.05, and this effect differed
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450
i
Schizophrenics / 400
J~ . , , ,_.....0 ,~
-
4) ~- 350
g
Controls
300 ...... 250
Figure 2. Endogenous cues: mean reaction times of schizophrenic subjects and controls for each cue condition. Loft visualfield Flightvisualfield
I
I
i
Neutral
Vatld
Invalid
Cue CondlUon
across groups, F (2,48) ffi 3.63, p < 0.03. As with the trend observed with exogenous cues, schizophrenics were overall slower than normals, F (1,24) ffi 4.68, p < 0.04, but there was no hint of an interval by field interaction nor an interval by field by group interaction, F < 1. Further group comparisons were therefore made collapsed across cuetarget interval. Mean reaction times for each cue condition for the two groups are presented in Figure 2. Analysis of costs (neutral versus invalid cue) revealed a main effect of validity, F (1,24) - 4.91, p ffi < 0.04, and a main effect of group, F (1,24) ffi 4.62, p < 0.04, with schizophrenic subjects once again showing longer reaction times overall. There was also a trend towards a significant group by field by validity interaction, F (1,24) = 3.52, p ffi 0.07. Because a left field advantage in schizophrenia has been hypothesized, we evaluated this trend with planned comparisons. For schizophrenic subjects there were significant costs for left visual field targets F (1,13) ffi 5.15, p ffi 0.04, whereas for right visual field targets no costs were evident, F < 1. In normals, significant costs were seen for targets in the right visual field, F (1,11) ffi 8.10, p < 0.02 but there was only a trend toward costs for left visual field targets, F (1,11) ffi 3.37, p ffi 0.09. In the analysis of benefits (neutral versus valid trials), there was a main effect of validity, F (1,24) ffi 36.24, p < 0.001, and again a main effect of group, F (1,24) 4.66, p < 0.04, with schizophrenics having longer reaction times overall than controls. No hint of a group by field by validity interaction was present, F < 1, NS. These findings suggest a performance asymmetry for effortful covert orienting in this group of schizophrenic subjects characterized by greater costs to invalidly cued left vi~,~ual field targets than to invalidly cued targets appearing in the right visual field. However, the right visual field disadvantage found with exogenous cues disappeared for neutral and valid conditions and was reversed for the invalid condition.
Discussion The results for the exogenous task provide further evidence for the presence of a left hemispheric deficit in information processing in schizophrenia. An analysis of the source of the significant group by field by interval interaction in the exogenously cued task
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indicated that automatic orienting to targets presented in the fight visual field at the 100msec interval was slower in schizophrenics than in normals. This finding is consistent with a deficit in visual spatial orienting mediated by the left hemisphere. The schizophrenic subjects in this study, who were all off medications, did not automatically attend to cues in the peripheral right visual field as readily as to cues in the left visual field. However, the pattern of performance with endogenous cuing suggests that the schizophrenic patients were able to use symbolic cues to control attention and largely overcome this particular lateraiized deficit. A possible confound in the comparison of the results of the two tasks in the current study is that their order of administration to subjects was not counterbalanced. This raises the possibility of fatigue leading to differential performance on the two tasks. As discussed in the Methods section, we did not counterbalance tasks to avoid biasing performance in the exogenously cued task with a prior probability manipulation. As the more general right visual field deficit reported here is seen with the exogenously cued task, which was given first, this particular finding is not subject to this potential confound. The findings with endogenous cues are consistent with those of Posner et al (1988) for validly cued conditions where these authors compared their findings to those obtained from studies of patients with lesions of the parietal lobe. Such patients can overcome contralesional delays when they are cued to the target location. Ever~ patients with full blown neglect can do so in validly cued trials (Morrow and Ratcliffc 1987). The ability to effortfully use attention is relatively intact in these neurologically damaged patients (Posner et al 1984). However, the pattern of asymmetry of costs for invalidly cued targets seen with endogenous cues is different from that reported in left parietal patients and different from that ~eported by Posner et al (1988) in their study of patients with schizophrenia. In left parietal patients, and in the schizophrenic subjects studied by Posner et al, costs were relatively larger for invalidly cued right visual field targets (left field cues) than invalidly cued left visual field targets (right field cues). In the present study the asymmetry in costs in the schizophrenic patients ran in the opposite direction, with greater costs for invalid left visual field targets than for invalid right visual field targets. There are a number of possible explanations for our finding a different pattern of asymmetry in costs to those reported in the Posner et al (1988) study. A recent report by Strauss et al (1991) of an absence of asymmetry of performance in a group of stable, treated and remitted schizophrenics suggests that cost asymmetry in the covert orienting task in schizophrenia may be a state-dependent phenomenon. All three untreated patients in the Posner et al (1988) study were subchronic or schizophreniform at the time of testing. The rest of the patients were subchronic or chronic and treated with a variety of medications. All patients were acutely psychotic. Tomer and Flor-Henry (1989) have demonstrated a reversal of asymmetrical hemi-neglect in acutely psychotic schizophrenic patients following a brief course of treatment with neuroleptic agents, with an initial right field deficit evolving into a left field deficit with drug treatment. Patients with Parkinsons disease (Wright et al 1990) and young normal subjects challenged with the neuroleptic droperidol (Clark et al 1988) show decreased costs associated with invalid cues when compared with normals and placebo challenges, respectively. Variability in dopamine activity during the course of the illness, with clinical state, or associated with the effects of treatment may account for the reversed asymmetry in costs which contrasts our findings with endogenous cues and the findings of Posner et al )88). Further studies comparing patients with schizopl ala at different phases in their
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illness, prospective studies of patients on and off medications, and studies of normals challenged with both dopamine agonist and antagonist drags, are needed to c,arify the role of each of the above factors in determining the pattern of costs and benefits in endogenously cued covert orienting of attention. Such studies are currently being initiated in our laboratory. Finally, a number of differences between our endogenous cuing paradigm and that used by Posner et al do not make the current study entirely comparable with previous studies. In the current study we used a neutral cue consisting of brightening of both central directional cues, whereas Posner et al (1988) used a no cue condition. It is possible that the occasional absence of a cue (as compared with simultaneous presence of both directional cues) may have produced a higher level of attentiveness in the Posner et al (1988) study. Posner's no cue condition was also less probable (20% of trials) than our neutral cue condition (one-third of trials), and this also could result in greater attentiveness in the former task. Higher levels of attentiveness may result in increased benefits and decreased costs for cues (Jonides and Mack 1984). Secondly, in contrast to the brightening of the peripheral boxes used by Posner et al, directional cues in the current study consisted of brightening of central directional cues. Thus, previous findings may reflect the effects of automatic visual orienting, inhibition of return, and controlled covert visual orienting, whereas the current study provides a more direct measure of automatic and controlled contributions to covertly directed visual spatial attention. These findings suggest that automatic orienting to endogenously cued targets is disrupted for right visual field targets in schizophrenia, consistent with left hemispheric attentional pathology in this illness. They also suggest that when schizophrenics are provided with cues that allow them to use attention strategically they are able to largely overcome this general right visual field attentional deficit. This study was supportedin part by VA MedicalResearchCouncilawardAA06637to LynnC. Robertsonand by NIMHGrant M.H. 46990 to Thomas E. Nordahl.
References Clark CR, Oeffen GM, Oeffen LB (1988): Catecholamines and the covert orientation of attention in humans. Neuropsychologia 27:131-139. Early TS, Posner MI, Reiman EM, Raichle ME (1989): Hyperactivity of the left striato-pallidal projection. Part I: Lower level theory. Psychol Dev 2:85-108. Henderson JM (1991): Stimulus discrimination following covert attentional orienting to an exogenous cue. J Exp Psychol 17(I):91-106. Jonides J, Mack R (1984): On the cost and benefit of cost and benefit. Psychol Bull 96(10:29-44. Kane J, Honigfield G, Singer J, Meltzer H (1988): Clozapine for the treatment-free schizophrenic. Arch Gen Psychiatry 45:789-796. Morrow LA, Ratcliffe G (1987): Attentional mechanisms in clinical neglect. J Clin Exp Neuropsychol 9:74-75. Muller HJ, Rabbitt P (1989): Reflexive and voluntary orienting of visual attention: Time course of activation and resistance to interruption. J Exp Psychol 15(2):315-330. Posner MI, Cohen Y (1984): Components of visual orienting. In Bouma H, Bouwhuis DG (eds), Attention and Performance. Hillsdale, NJ: Erlbaum, pp 531-556. Posner MI, Early TS (19°0): What's left of attention in schizophrenia. Arch Gen Psychiatry 47(4):394.
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Posner MI, Peterson SE (1990): The attention system of the human brain. Annu Rev Neurosci 13:25-42. Posner MI, Walker JA, Frieclrich FJ, Rafal RD (1984): Effects of parietal lobe injury on the covert orienting of visual attention. J Neurosci 4:1863-1874. Posner MI, Early TS, Reiman E, Pardo PJ, Dhawan M (1988): Asymmetries of attentional control in schizophrenia. Arch Gen Psychiatry 45:814-821. Rafai RD, Calahresi PA, Brennan CW, Sciolto TK (1989): Saccade preparation inhibits reorienting to recently attended locations. J Exp Psychol 15(4):673-685. Robertson LC, Lamb MR, Knight RT (1988): Effects of lesions of temporo-parietai junction on perceptual and attentional processing in humans. J Neurosci 10:3757-3769. Spitzer R, Williams JW (1987): Structured clinical interview for DSM-III, revised version. New York, NY: New York Psychiatric Institute. S~r~e~ ,~,~E,Novakovic T, Tien AY, Bylsma F, Pearlson GD (1991): Disengagement of attention in schizophrenia. Psychiatry Res 37:139-146. Tomer R, Flor-Henry P (1989): Neuroleptics reverse attention asymmetries in schizophrenic patients. Biol Psychiatry 25:852-860. Wright MJ, Bums RJ, Geffen GM, Geffen LB (1990): Covert orientation of visual attention in Parkinsons disease: An impairment in the maintenance of attention. Neuropsychologia 28(2):151159.